Fearful symmetry in aposematic plants

Abstract

Symmetry has been proposed to increase the efficiency of visual aposematic displays in animals, and I suggest that it may also be true for many aposematic spiny or poisonous plants. For instance, in the very spiny plant taxa cacti, Aloe sp., Agave sp. and Euphorbia sp., which have been proposed to be aposematic because of their colorful spine system, the shoots, and in cacti, the spiny fruits as well, are usually radially symmetric. Moreover, in the radial symmetric shoots of Agave and Aloe their individual spiny leaves are also bilaterally symmetric. Spiny or poisonous fruits of various other taxa, the symmetric spiny leaf rosettes and flowering spiny heads of many Near Eastern species of the Asteraceae and other taxa, and poisonous colorful flowers in taxa that were proposed to be aposematic are also symmetric. Thus, in plants, like in animals, symmetry seems to be commonly associated with visual aposematism and probably contributes to its effectiveness. Symmetry may stem from developmental constraints, or like in flowers, have other signaling functions. However, because of the better perception of symmetry by animals it may exploit inherited modes of animal sensing that probably result in paying more attention to symmetric shapes. All these possible alternatives do not negate the probable deterring role of symmetry in plant aposematism.

The aboveground parts of plants are commonly utilized as food by various types of visually oriented herbivores.¹ Thus, there is a permanent evolutionary arms race between plants and their herbivores in which, on an evolutionary time scale, plants acquire better defenses and herbivores partly or fully overcome them.² One of the proposed defense methods of toxic or spiny plants against herbivory is visual aposematism (warning coloration).^3-8

Aposematic coloration, a well-known phenomenon in animals, has until recently been given very little attention in plants. Often, a brightly-colored (red, orange, yellow, white with black markings or combinations of these colors) animal is dangerous or unpalatable to predators, a trait that confers a selective advantage because predators learn to associate the coloration with unpleasant qualities and avoid such organisms.^7,9-12

In plants, visual aposematism was first proposed to defend poisonous ones.^3,4,13 Only recently has it been proposed that colorful spines and associated conspicuous coloration patterns are cases of vegetal aposematic coloration analogous to such coloration in poisonous or dangerous animals, and that spine colors or associated patterns of coloration communicate between plants and potential herbivores.^5-7,14-19 The study of plant aposematism lags far behind that of animals^6,8 and here I wish to bridge one of these gaps.

Forsman and Merilaita²⁰ and Forsman and Herrström²¹ proposed that symmetry increases the efficiency of visual aposematic displays in animals. This hypothesis was contested with the hypothesis that asymmetry impairs the efficiency of visual aposematism while increasing the defensive value of cryptic color patterns.²² Forsman and Merilaita²² compared intra-individual asymmetry in color patterns of cryptic patterns on fore wings and aposematic patterns on hind wings of three species of moths. They found somewhat larger asymmetry in cryptic patterns but it was not significant and therefore concluded that there were probably developmental or genetic constraints on the evolution of pronounced asymmetry in the system they studied. In the cuttlefish Sepia officinalis Langridge²³found that color changes that enhanced crypsis were symmetrical while those that enhanced anti-predator signaling were asymmetrical, contrary to the theoretical predictions. These results indicate that understanding the role of symmetry in both crypsis and aposematism is not straightforward. Recently, Stevens et al.²⁴ showed that asymmetry in warning signals may not be costly to prey compared with other features of the aposematic signal, such as color and overall size. However, there is an innate preference for symmetry in the visual system of animals, probably because of the need to recognize objects,²⁵ a well-known fact from pollination biology.²⁶

Here I review various cases of putative visual aposematism in plants and show that symmetry characterizes many of them. This, however, is by no means proof that symmetry in these plants evolved because of aposematic signaling, but rather that such signaling may be stronger when associated with symmetry.

Although it has received very little attention even in zoology, symmetry has been proposed to increase the efficiency of visual aposematic displays in animals,^20,21 although the role of symmetry in aposematism is not global.^23,24 A careful examination of the major plant taxa and plant organs proposed to be visually aposematic shows a good agreement with the zoological hypothesis for symmetry increasing the effect of aposematism in animals.

(I) Toxic colorful flowers, which were one of the first plant parts proposed to be aposematic,^3,6 are typically symmetric.^26,27 (II) Similarly, putative aposematic toxic fruits^28,29 and spiny unripe red fruits that were also proposed to be aposematic²⁹ are symmetric. (III) Many putatively aposematic spiny plants are wholly symmetric, or their aposematic organs are symmetric. The spiniest plant taxa (cacti, Aloe sp, Agave sp, Euphorbia sp), which have been proposed to be aposematic because of their colorful spine system,⁵ their shoots, and in cacti the very spiny colorful and conspicuous fruits as well, are commonly radial symmetric. Moreover, in Agave and Aloe, the individual spiny leaves are commonly bilaterally symmetric. In many cacti species, the spines are arranged along the symmetrically arranged stem ribs or evenly distributed over flat cladode areas, and in Euphorbia sp they are arranged along the stem in symmetric pairs. The same is true for the spiny leaf rosettes and flowering spiny heads of the many East Mediterranean species of the Asteraceae³⁰ that are symmetric.

Thus, like in certain animals,^20,21 visual aposematism in spiny and poisonous plants also seems to be commonly associated with symmetry. This association may be the outcome of developmental constraints, or in flowers and fruit with other signaling systems for gene dispersal, as well as with perceptual exploitation of animal sensing sensu Schaefer and Ruxton,³¹ because animals probably pay more attention to symmetric shapes.^25,26

There is an obvious need for experimental testing of the role of symmetry in visual plant aposematism. This need is part of the general great need to test hypotheses of plant aposematism, a subject that has received too little theoretical and experimental attention in comparison to animal aposematism.^6,31 However, it is probable that since aposematism in general and symmetry-related in particular, is only one of several defensive components of plants (and animals), it will be very difficult to single out the role of symmetry in direct defense from herbivores.